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Research ArticleFUNCTIONAL

Altered Processing of Complex Visual Stimuli in Patients with Postconcussive Visual Motion Sensitivity

J.W. Allen, A. Trofimova, V. Ahluwalia, J.L. Smith, S.A. Abidi, M.A.K. Peters, S. Rajananda, J.E. Hurtado and R.K. Gore
American Journal of Neuroradiology February 2021, DOI: https://doi.org/10.3174/ajnr.A7007
J.W. Allen
aFrom the Departments of Radiology and Imaging Sciences (J.W.A., A.T., J.L.S.)
bNeurology (J.W.A.)
dWallace H. Coulter Department of Biomedical Engineering (J.W.A., R.K.G.), Georgia Institute of Technology and Emory University, Atlanta, Georgia
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A. Trofimova
aFrom the Departments of Radiology and Imaging Sciences (J.W.A., A.T., J.L.S.)
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V. Ahluwalia
eGeorgia State University/Georgia Tech Center for Advanced Brain Imaging (V.A.), Atlanta, Georgia
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J.L. Smith
aFrom the Departments of Radiology and Imaging Sciences (J.W.A., A.T., J.L.S.)
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S.A. Abidi
cSchool of Medicine (S.A.A.), Emory University, Atlanta, Georgia
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M.A.K. Peters
fDepartment of Bioengineering (M.A.K.P., S.R.), University of California, Riverside, Riverside, California
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S. Rajananda
fDepartment of Bioengineering (M.A.K.P., S.R.), University of California, Riverside, Riverside, California
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J.E. Hurtado
gShepherd Center (J.E.H., R.K.G.), Atlanta, Georgia
hShepherd Center (J.E.H., R.K.G.), Atlanta, Georgia
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R.K. Gore
dWallace H. Coulter Department of Biomedical Engineering (J.W.A., R.K.G.), Georgia Institute of Technology and Emory University, Atlanta, Georgia
gShepherd Center (J.E.H., R.K.G.), Atlanta, Georgia
hShepherd Center (J.E.H., R.K.G.), Atlanta, Georgia
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Abstract

BACKGROUND AND PURPOSE: Vestibular symptoms are common after concussion. Vestibular Ocular Motor Screening identifies vestibular impairment, including postconcussive visual motion sensitivity, though the underlying functional brain alterations are not defined. We hypothesized that alterations in multisensory processing are responsible for postconcussive visual motion sensitivity, are detectable on fMRI, and correlate with symptom severity.

MATERIALS AND METHODS: Twelve patients with subacute postconcussive visual motion sensitivity and 10 healthy control subjects underwent vestibular testing and a novel fMRI visual-vestibular paradigm including 30-second “neutral” or “provocative” videos. The presence of symptoms/intensity was rated immediately after each video. fMRI group-level analysis was performed for a “provocative-neutral” condition. Z-statistic images were nonparametrically thresholded using clusters determined by Z > 2.3 and a corrected cluster significance threshold of P = .05. Symptoms assessed on Vestibular Ocular Motor Screening were correlated with fMRI mean parameter estimates using Pearson correlation coefficients.

RESULTS: Subjects with postconcussive visual motion sensitivity had significantly more Vestibular Ocular Motor Screening abnormalities and increased symptoms while viewing provocative videos. While robust mean activation in the primary and secondary visual areas, the parietal lobe, parietoinsular vestibular cortex, and cingulate gyrus was seen in both groups, selective increased activation was seen in subjects with postconcussive visual motion sensitivity in the primary vestibular/adjacent cortex and inferior frontal gyrus, which are putative multisensory visual-vestibular processing centers. Moderate-to-strong correlations were found between Vestibular Ocular Motor Screening scores and fMRI activation in the left frontal eye field, left middle temporal visual area, and right posterior hippocampus.

CONCLUSIONS: Increased fMRI brain activation in visual-vestibular multisensory processing regions is selectively seen in patients with postconcussive visual motion sensitivity and is correlated with Vestibular Ocular Motor Screening symptom severity, suggesting that increased visual input weighting into the vestibular network may underlie postconcussive visual motion sensitivity.

ABBREVIATIONS:

BESS
Balance Error Scoring System
DHI
Dizziness Handicap Inventory
FEF
frontal eye fields
MT/V5
middle temporal visual area
PCSS
Post Concussion Symptom Scale
PCVMS
postconcussive visual motion sensitivity
PIVC
parietoinsular vestibular cortex
VOMS
Vestibular Ocular Motor Screening
VVAS
Visual Vertigo Analog Scale

Footnotes

  • This work was supported by the Georgia State/Georgia Tech Center for Advanced Brain Imaging Neural Engineering Center Seed Grant and the Emory University Department of Radiology and Imaging Sciences Seed Grant.

  • Disclosures: Jason W. Allen—RELATED: Grant: Georgia State/Georgia Tech Center for Advanced Brain Imaging Neural Engineering Center Seed Grant and Emory University Department of Radiology and Imaging Sciences Seed Grant.* Anna Trofimova—RELATED: Grant: Georgia State/Georgia Tech Center for Advanced Brain Imaging Neural Engineering Center Seed Grant and Emory University Department of Radiology and Imaging Sciences Seed Grant*; UNRELATED: Grants/Grants Pending: Radiological Society of North America Research and Education Foundation Resident Research Grant.* Jeremy L. Smith—RELATED: Grant: Georgia State/Georgia Tech Center for Advanced Brain Imaging Neural Engineering Center Seed grant and Emory University Department of Radiology and Imaging Sciences Seed Grant.*; UNRELATED: Consultancy: Bold & Stark LC, Comments: rodent data analysis for Albert Einstein College of Medicine. Julia E. Hurtado—UNRELATED: Employment: Shepherd Center. Russell K. Gore—RELATED: Grant: Shepherd Center, Comments: Georgia State/Georgia Tech Center for Advanced Brain Imaging Neural Engineering Center Seed Grant and Emory University Department of Radiology and Imaging Sciences Seed Grant; funding for imaging and subject reimbursement; I was not compensated for the effort*; UNRELATED: Employment: Shepherd Center, Comments: employed physician; Grants/Grants Pending: Shepherd Center, Comments: Arthur M. Blank Family Foundation Grant.* *Money paid to the institution.

  • Paper previously presented, in part, at: Annual Meeting of the American Society of Neuroradiology May 18–23, 2019; Boston, Massachusetts.

  • © 2021 by American Journal of Neuroradiology
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Altered Processing of Complex Visual Stimuli in Patients with Postconcussive Visual Motion Sensitivity
J.W. Allen, A. Trofimova, V. Ahluwalia, J.L. Smith, S.A. Abidi, M.A.K. Peters, S. Rajananda, J.E. Hurtado, R.K. Gore
American Journal of Neuroradiology Feb 2021, DOI: 10.3174/ajnr.A7007

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Altered Processing of Complex Visual Stimuli in Patients with Postconcussive Visual Motion Sensitivity
J.W. Allen, A. Trofimova, V. Ahluwalia, J.L. Smith, S.A. Abidi, M.A.K. Peters, S. Rajananda, J.E. Hurtado, R.K. Gore
American Journal of Neuroradiology Feb 2021, DOI: 10.3174/ajnr.A7007
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